Sexual selection may support phenotypic plasticity in male coloration of an African cichlid fish.

The expression of sexually selected traits, such as ornaments or body coloration, is often influenced by environmental conditions. While such phenotypic plasticity is often thought to precede evolutionary change, plasticity itself can also be a target of selection. However, the selective forces supporting the evolution and persistence of plasticity in sexual traits are often unclear. Using the cichlid fish Astatotilapia burtoni, we show that variation in the level of mate competition may promote plasticity in body coloration. In this species, males can change between yellow and blue colour. We found that experimentally increased competition over mating territories led to a higher proportion of males expressing the yellow phenotype. The expression of yellow coloration was found to be beneficial because yellow males won more staged dyadic contests and exhibited a lower level of oxidative stress than blue males. However, females were more likely to spawn with blue males in mate choice experiments, suggesting that expression of blue coloration is sexually more attractive. The ability to adjust colour phenotype according to the local competitive environment could therefore promote the persistence of plasticity in coloration.

Social status influences relationships between hormones and oxidative stress in a cichlid fish.

An individual's social environment can have widespread effects on their physiology, including effects on oxidative stress and hormone levels. Many studies have suggested that variation in oxidative stress experienced by individuals of different social statuses might be due to endocrine differences, however, few studies have evaluated this hypothesis. Here, we assessed whether a suite of markers associated with oxidative stress in different tissues (blood/plasma, liver, and gonads) had social status-specific relationships with circulating testosterone or cortisol levels in males of a cichlid fish, Astatotilapia burtoni. Across all fish, blood DNA damage (a global marker of oxidative stress) and gonadal synthesis of reactive oxygen species [as indicated by NADPH-oxidase (NOX) activity] were lower when testosterone was high. However, high DNA damage in both the blood and gonads was associated with high cortisol in subordinates, but low cortisol in dominants. Additionally, high cortisol was associated with greater production of reactive oxygen species (greater NOX activity) in both the gonads (dominants only) and liver (dominants and subordinates). In general, high testosterone was associated with lower oxidative stress across both social statuses, whereas high cortisol was associated with lower oxidative stress in dominants and higher oxidative stress in subordinates. Taken together, our results show that differences in the social environment can lead to contrasting relationships between hormones and oxidative stress.

Social dominance and reproduction result in increased integration of oxidative state in males of an African cichlid fish.

Oxidative stress is a potential cost of social dominance and reproduction, which could mediate life history trade-offs between current and future reproductive fitness. However, the evidence for an oxidative cost of social dominance and reproduction is mixed, in part because organisms have efficient protective mechanisms that can counteract oxidative insults. Further, previous studies have shown that different aspects of oxidative balance, including oxidative damage and antioxidant function, vary dramatically between tissue types, yet few studies have investigated oxidative cost in terms of interconnectedness and coordination within the system. Here, we tested whether dominant and subordinate males of the cichlid Astatotilapia burtoni differ in integration of different components of oxidative stress. We assessed 7 markers of oxidative stress, which included both oxidative damage and antioxidant function in various tissue types (total of 14 measurements). Across all oxidative stress measurements, we found more co-regulated clusters in dominant males, suggesting that components of oxidative state are more functionally integrated in dominant males than they are in subordinate males. We discuss how a high degree of functional integration reflects increased robustness or efficiency of the system (e.g. increased effectiveness of antioxidant machinery in reducing oxidative damage), but we also highlight potential costs (e.g. activation of cytoprotective mechanisms may have unwanted pleiotropic effects). Overall, our results suggest that quantifying the extent of functional integration across different components of oxidative stress could reveal insights into the oxidative cost of important life history events.

Social instability influences rank-specific patterns of oxidative stress in a cichlid fish.

In many animal societies, dominant individuals have priority access to resources. However, defending high rank can be costly, especially in unstable social hierarchies where there is more intense competition. Oxidative stress has been proposed as a potential cost of social dominance, but few studies have examined this cost in relation to social stability. We studied the cost of social dominance in the cichlid fish Astatotilapia burtoni by manipulating social stability among males in replicate naturalistic communities for 22 weeks. We found that our social stability treatment influenced status-specific patterns in 3 out of 6 measurements of oxidative stress. Specifically, dominant males experienced increased plasma oxidative damage (measured as reactive oxygen metabolites, ROMs) compared with subordinate males in stable hierarchies only. Subordinate males in unstable hierarchies had higher ROMs than their stable community counterparts, but we found no effect of social stability treatment for dominant males. However, dominant males tended to have reduced total antioxidant capacity (TAC) in the liver when compared with subordinate males in unstable hierarchies, suggesting that the cost of social dominance is higher in unstable hierarchies. There were no effects of status and treatment on gonad TAC, muscle TAC or oxidative DNA damage. We conclude that the stability of the social environment influences the relative cost of social dominance in a tissue- and marker-specific manner.

How does male-male competition generate negative frequency-dependent selection and disruptive selection during speciation?

Natural selection has been shown to drive population differentiation and speciation. The role of sexual selection in this process is controversial; however, most of the work has centered on mate choice while the role of male-male competition in speciation is relatively understudied. Here, we outline how male-male competition can be a source of diversifying selection on male competitive phenotypes, and how this can contribute to the evolution of reproductive isolation. We highlight how negative frequency-dependent selection (advantage of rare phenotype arising from stronger male-male competition between similar male phenotypes compared with dissimilar male phenotypes) and disruptive selection (advantage of extreme phenotypes) drives the evolution of diversity in competitive traits such as weapon size, nuptial coloration, or aggressiveness. We underscore that male-male competition interacts with other life-history functions and that variable male competitive phenotypes may represent alternative adaptive options. In addition to competition for mates, aggressive interference competition for ecological resources can exert selection on competitor signals. We call for a better integration of male-male competition with ecological interference competition since both can influence the process of speciation via comparable but distinct mechanisms. Altogether, we present a more comprehensive framework for studying the role of male-male competition in speciation, and emphasize the need for better integration of insights gained from other fields studying the evolutionary, behavioral, and physiological consequences of agonistic interactions.